Directory UMM :Data Elmu:jurnal:A:Applied Soil Ecology:Vol13.Issue1.Sep1999:

Applied Soil Ecology 13 (1999) 69±86

Nematode communities as indicators of status and processes of a
soil ecosystem in¯uenced by agricultural management practices
D.L. Porazinskaa,*, L.W. Duncanb, R. McSorleyc, J.H. Grahamb
a
Natural Resource Ecology Laboratory, Ft. Collins, CO 80523, USA
Citrus Research and Education Center, University of Florida, Lake Alfred, FL 33850-2299, USA
c
Department of Entomology and Nematology, University of Florida, P.O. Box 110620, Gainesville, FL 32611-0620, USA
b

Accepted 7 April 1999

Abstract
Nematode communities were monitored for three years in a citrus soil ecosystem in Central Florida under various agricultural
regimes comparing standard vs. reduced-input practices. Differences in agricultural regimes consisted of two fertilization
levels, two irrigation levels, and two types of ground cover under the tree (herbicide vs. mulch). While some nematodes were
affected sporadically by fertilization and irrigation treatments, mulch had a consistent and frequently signi®cant effect on
many bacterivores, fungivores, herbivores, and omnivores. Rhabitidae, Cephalobus, Aphelenchus, and Aphelenchoides had an
immediate but temporary response to mulch additions. Acrobeles, Acrobeloides, Eucephalobus, Teratocephalus,

Criconemoides, Aporcelaimellus, and Eudorylaimus were always less abundant in mulch-treated plots, whereas Plectus and
Belonolaimus were always more abundant. Of various indices of community composition, only maturity indices, unlike
diversity indices, indicated the status and intensity of soil processes (decomposition, mineralization). However, different
responses of single genera within a trophic group implied unique contributions of nematode genera in soil ecosystem
processes on a temporal scale, suggesting that generic or possibly species level of resolution provide the most adequate
information about the soil ecosystem. # 1999 Elsevier Science B.V. All rights reserved.
Keywords: Agricultural practices; Bioindicator; Citrus; Diversity; Ecological indices; Maturity index; Nematode community; Soil ecosystem;
Sustainability; Sustainable agriculture; Trophic group

1. Introduction
Several characteristics of soil nematodes make
them good candidates for bioindicators of the status
and processes of an ecosystem. Nematodes possess the
most important attributes of any prospective bioindicator (Cairns et al., 1993): abundance in virtually all

*Corresponding author. Tel.: +1-970-491-5599; fax: +1-970491-1965; e-mail: dorota@nrel.colostate.edu

environments, diversity of life strategies and feeding
habits (Freckman, 1988; Yeates et al., 1993a), short
life cycles, and relatively well-de®ned sampling procedures. For these reasons, several researchers have

attempted to develop relationships between nematode
community structure and succession of natural ecosystems or environmental disturbance (Ettema and
Bongers, 1993; Freckman and Ettema, 1993; Freckman and Virginia, 1997; De Goede and Dekker, 1993;
Wasilewska, 1994; Yeates and Bird, 1994). In general,
nematode communities or ecological indices derived

0929-1393/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved.
PII: S 0 9 2 9 - 1 3 9 3 ( 9 9 ) 0 0 0 1 8 - 9

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D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

from them re¯ected differences between undisturbed
and human-impacted environments.
Conventional farming systems have been associated
with many environmental ills. Common problems
such as loss of soil fertility, soil erosion, reduction
of soil biodiversity, and ground water pollution (Ehrlich, 1988) may become crucial issues affecting production of suf®cient amounts of food and ®ber. A key
to success of sustainable agriculture (Schaller, 1993)

will be conservation of natural resources and higher
dependence on natural ecosystem processes (Elliot
and Cole, 1989).
The ability to monitor and assess the quality of
agroecosystem soils would be of signi®cant importance, particularly to farm managers, who could modify their farming strategies accordingly. The idea that
changes in the soil environment imposed by agricultural management practices could be revealed by
measures of nematode community patterns has been
investigated in recent years (Ferris et al., 1996; Freckman and Ettema, 1993; McSorley and Frederick,
1966; Porazinska et al., 1998a; Yeates et al., 1997).
The more challenging task still to be undertaken is
interpretation of those patterns. For instance, quanti®cation of diversity or maturity indices for simple
ecosystem comparisons is of limited value. Any
assumption that reduced diversity negatively affects
stability and thus sustainability of agroecosystems
needs to be validated. Components of sustainability
of agroecosystems and natural ecosystems may differ.
For example, Porazinska et al. (1998b) found maturity
indices of nematode communities positively correlated with irrigation levels, but negatively correlated
with fruit production and pro®tability of a citrus
orchard in Florida, U.S.A. Higher maturity indices

indicated better environments for nematode K-strategists, but were achieved through overuse of water
resources. Thus, it is important to ®nd trends illustrating the soil condition, but more important to ®nd their
explanation. Only this type of information would
allow us to use our knowledge of a relationship
between soil biodiversity and some measures of an
ecosystem (energy use, disturbance, pro®tability, or
resource conservation) to increase its sustainability.
The objectives of this study were to:
1. characterize nematode communities (taxonomic
and ecological index description) in soils exposed

to different agricultural management practices
(under same physico-chemical soil properties,
vegetation cover, and climatic conditions);
2. evaluate whether soil ecosystem differences
imposed by farming tactics can be reflected by
nematode characterization (key taxa or indices)
3. determine which measures of ecological characterization are the most useful in differentiating various agricultural regimes; and
4. determine which of the ecological measures most
adequately illustrate conditions of the soil environment exposed to different farming practices.

2. Material and methods
2.1. Site description
The experimental site was located on the property
of the University of Florida Citrus Research and
Education Center (CREC) in Lake Alfred, Florida
(28860 N, 818450 W). The soil is characterized as
Astatula ®ne sand with pH 6.2% and 1.2% organic
matter. The experimental site had been previously (70
years) planted with citrus trees (Citrus spp. ). In 1986,
young citrus trees of `Hamlin' orange (Citrus sinensis
(L) Osbeck) on `Cleopatra' mandarin (C. reticulata)
were planted in rows 6 m apart with 4.6 m between
trees within rows. On 2 February 1995, 32 trees of
similar size (5 m height) and vigor were chosen and
preliminary soil samples collected to determine baseline data. A 2  2  2 factorial experiment was established, involving two fertilization levels, two irrigation
levels, and two types of ground cover under the tree.
The eight treatment combinations were replicated four
times, in four blocks based on densities of the plant
parasites Belonolaimus spp. and Phytophthora nicotianae Breda de Haan (Timmer et al., 1988) in the

preliminary soil samples. Individual plots (one tree per
plot) were fertilized either with the amount of N
typically used (336 kg N/ha/year) or reduced amount
of nitrogen (168 kg N/ha/year) divided over six applications: February, March, April, May, August, and
October. The N was applied as a granular 8 : 4 : 8
(N : P2O5 : K2O) fertilizer. For the reduced nitrogen
treatment, phosphorus and potassium applications
were also reduced to maintain the 8 : 4 : 8 ratio
(changes of the N : P : K ratio interfere with N uptake

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

by citrus roots). Water was delivered to trees through a
microsprinkler irrigation system. Plots receiving the
standard amount of water were irrigated twice a week,
typically on Mondays and Fridays during spring,
summer, and fall (except raining days), and once a
week in winter. The duration of irrigation was always
the same. When the water potential (at depth of 15 cm
in the soil pro®le) in plots receiving the reduced

amount of water would drop to approximately
ÿ15 kPa, trees would be irrigated in the same manner
as the trees in the standard water treatments. To
control the weed growth under the tree canopies, plots
received either the standard herbicide glyphosate (N(phosphonomethyl) glycine, isopropylamine salt) or
mulch (alternative to herbicide practice). Generally,
glyphosate was applied as 2.2 kg ai in 467.7 l water/ha
three times a year: March, June, and October. Mulch
was obtained from Bedmister Bioconversion, Sevierville, TN. The mulch contained 90% municipal waste
compost with almost no visible inert material (glass,
plastic, etc.) and 10% wastewater residual (Widmer et
al., 1997). The compost was high in calcium and thus
slightly alkaline (Table 1) (Widmer et al., 1997). The
C : N ratio was 19.3. Although heavy metal concen-

Table 1
Analysis of municipal solid waste compost
Element

Composition

pH

7.52

C
N

%
29.12
1.61

C : N ratio

19.3

P
Ca
Mg
K

mg gÿ1
2.9
24.8
2.4
3.4

Zn
Cu
Mn
Fe
Cd
Pb
Ni

mg gÿ1
423
165
210
8805

2
212
34

Modified from Widmer et al., 1997.

71

trations seemed to be relatively high, the municipal
compost waste met the U.S. Environmental Protection
Agency's criteria for exceptional quality (U.S. Environmental Protection Agency, 1990). A layer of ca.
10 cm of mulch was spread evenly under the tree
canopy (from tree stem to tree drip line) on 4 April
1995. The same procedure was repeated approximately two years later on 27 May 1997 using the
same batch mulch.
2.2. Sampling and extraction
Soil samples were collected at approximately
three-month intervals for three years (11 times): 2
February 1995 (baseline), 8 May 1995, 19 September
1995, 10 February 1996, 9 May 1996, 3 September

1996, 19 December 1996, 1 April 1997, 3 June 1997,
26 September 1997, and 21 December 1997. Each
soil sample consisted of 16 cores (2 cm in diameter
and 30 cm length). Soil cores were taken from the
area delimited by the tree canopy shade and the
tree stem, with four cores 20 cm apart along each
half diagonal. Immediately before insertion of the
core into the soil pro®le, mulch was moved to
expose the soil surface. Mulch was replaced once
soil sampling was accomplished. The soil cores were
mixed and passed through a sieve (2 mm  2 mm
mesh size) to separate the roots from the soil. A soil
subsample of 100 cm3 was used immediately to
estimate populations of Phytophthora nicotianae, a
pathogen causing citrus root decay (Timmer et al.,
1988). The remaining soil was transported to
Gainesville, FL in sealed plastic bags and then stored
at 108C for no longer than 15 h. Nematodes were
extracted from 100 cm3 soil subsamples by wet
sieving followed by centrifugation (Jenkins, 1964).
The extracted nematodes were killed with heat
(4±5 min at 608C), identi®ed to genus, and counted
under an inverted microscope.
To estimate root biomass, citrus roots were separated from soil, washed and dried in an oven for ca.
96 h at 608C. From each soil sample, 4±8 g of soil was
dried to constant weight in an oven at 608C to determine soil moisture. Fungal and bacterial population
densities in soils collected on 1 April 1997, 3 June
1997, and 26 September 1997 were estimated using a
dilution plate method (Casida, 1968; Johnson and
Curl, 1972). Yearly fruit yield was determined from

72

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

citrus harvests taken on 6 December 1995, 13 February 1997, and 15 January 1998.
2.3. Nematode measures
The total number of nematodes in each genus, the
total number of nematodes of different genera, and the
total number of genera (richness) were recorded for
every soil sample. All nematode genera were assigned
to seven trophic groups: algivores; bacterivores; fungivores; omnivores; plant associates; plant parasites;
and predators (Yeates et al., 1993a). The total number
of nematodes in every trophic group and the percentage of every trophic group within the nematode
community were also recorded.
Based on the densities of genera and trophic groups,
ecological indices of the nematode community were
derived. The Shannon±Weaver diversity index (Shannon and Weaver, 1949) was used to compare diversity
of either genera or trophic groups, and Simpson (1949)
index was used to compare either generic or trophic
dominance. An additional measure of diversity was
derived from a reciprocal transformation of the Simpson's index (Freckman and Ettema, 1993). Maturity
indices sensu Bongers (1990) and sensu Yeates (1994)
were also calculated. The maturity index is a semiquantitative measure since it takes into consideration
biological and ecological characteristics of individual
nematode species comprising a particular community.
Nematodes at the family level are ranked on a c±p
scale from 1 (colonizer) to 5 (persister) illustrating
their life and feeding strategies and, presumably, the
conditions of the surrounding environment (Bongers,
1990). The maturity index is calculated as a weighted
mean of the c±p values of nematodes in the sample.
Bongers (1990) de®ned two types of maturity indices:
MI which includes nematodes belonging to all feeding
types except herbivores, and PPI which includes herbivores only. Yeates (1994) combined those two into
one total maturity index (TMI). In general, the higher a
maturity index value, the more mature and stable the
ecosystem. Fungivore-to-bacterivore ratio (Freckman
and Ettema, 1993) and fungivores ‡ bacterivores to
plant parasites ratio (Wasilewska, 1994) were calculated to compare decomposition and nutrient mineralization pathways and primary production. More
details on derivation of all the above ecological indices
are given elsewhere (Porazinska et al., 1998a).

2.4. Statistical analysis
The effects of different agricultural practices (two
levels of fertilizer, two levels of irrigation, and two
levels of ground cover) on the measures of nematode
genera and community structure were analyzed by
two methods: repeated measures which includes
split-plot in time analysis as well as ANOVA procedure for each separate date using SAS software (SAS
Institute, Cary, NC). Since the two methods revealed
similar results, ANOVA results were used for data
presentation and discussion. In addition, canonical
discriminant analysis on taxonomic description of
nematode communities was performed for treatment
separation.

3. Results
Although water and fertilization levels only occasionally affected a selected number of nematode
genera and nematode community indices, mulch
had more consistent and frequent effects on many
nematode measures throughout the entire time of the
experiment (Table 2). Discriminant analysis con®rmed the univariate analysis results. The ®rst canonical explained 35% of the total variation and
separated mulch from herbicide treatments (Fig. 1).
For the above reason, this paper will emphasize the
in¯uence of compost additions on the nematode community structure.

Fig. 1. View of treatments separated by the first canonical into two
groups: mulch plots (bars with positive values of the first
canonical) and herbicide treatments (bars with negative values of
the first canonical). M ˆ mulch, nM ˆ no mulch, rF ˆ reduced
amount of fertilizer, sF ˆ standard amount of fertilizer, rW ˆ reduced amount of water, sW ˆ standard amount of water.

73

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

Table 2
Occurrence of significant effects of water (W), mulch (M), and fertilizer (F) treatments, and their interactions on single nematode populations,
trophic groups, ecological indices, and other biological and physical characteristics of the soil environment
Water
Genus or family
Bacterivores
Rhabditidae
Monhysterida
Acrobeles
Acrobeloides
Cephalobus
Eucephalobus
Plectus
Zeldia
Prismatolaimus
Teratocephalus
Wilsonema
Misc. bacterivores

Fertilizer

W*M

W*F

******

*

*
*
*
**

W*M*F

*

****
**
**
**
******
**
***
***

*
**

**
*
*
*

***
**

*

**

**
*
**
**
*

*

*

**
*

*

**
***

**

**

*

Algivores
Chromadorida

**

***
*

*

Omnivores
Eudorylaimus
Aporcelaimellus
Dorylaimidae

*
**

*
**
*

*

Plant associates
Tylenchidae

**

***

*

*

*

***
*
**

*

*

*

Herbivores
Belonolaimus
Hoplolaimus
Criconemoides
Trophic groupsa
Bacterivores
Fungivores
Predators
Omnivores
Total
B/T
F/T
B‡F/T
A/T
P/T
O/T
Tl/T

M*F

**

Fungivores
Aphelenchus
Aphelenchoides
Predators
Prionchulus
Predatory dorylaims
Predatory mononchs

Mulch

*

*

*
**
**

*

**

**
***
**
*

*

*
**
*

***
***
**
**
*
*
***
*

**
*

*

*

***

*
*
*
*

*

**
*

**
*
*
*

74

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

Table 2 (Continued )
Water

Fertilizer

W*M

*

*
*

*

**
***
***
***
*
***
***
***
*****
*****
*****

**
*

***
**

**
**

H/T
B‡F
Ecological indicesb
Richness
F/B
B‡F/H
H0t
t
H0g
g
1/g
MI
TMI
PPI
Other variables
Moisture
Phytophthora
Root weight
Fungic
Bacteriac
Yieldc

Mulch

W*F

M*F

W*M*F

*
****

*

*

*

*
*

**
**

*
*
*
*

*
*

**
***
**
*

*

*

*

*
***

a

B ˆ bacterivores; F ˆ fungivores; A ˆ algivores; P ˆ predators; O ˆ omnivores; Tl ˆ tylenchids; H ˆ herbivores; T ˆ total.
Ht0 ˆ Shannon±Weaver trophic diversity; t ˆ Simpson trophic dominance; Hg0 ˆ Shannon±Weaver generic diversity; g ˆ Simpson generic
dominance; 1=0g ˆ Simpson generic diversity; MI ˆ maturity index; TMI ˆ total maturity index; PPI ˆ plant parasitic index.
c
Only three sampling dates for these measures.
Each asterisk (*) represents a sampling date (out of 11 total dates) on which a significant (at p  0.05) treatment effect or interaction existed.
b

3.1. Nematode populations
Total numbers of nematodes ranged from 359 to 821
per 100 cm3 in treatments without mulch, and from
412 to 1396 per 100 cm3 in treatments with mulch
additions (Fig. 2(a)). Within mulch treated plots, total
numbers of nematodes increased 3±4 weeks after each
mulch application. After the ®rst mulch addition, the
effect of compost on total nematode numbers was very
brief and lasted less than three months. The second
mulch treatment in 1997 resulted in signi®cantly
(p  0.05) higher nematode numbers for at least seven
months (three consecutive sampling events). This
pattern was driven mostly by bacterivorous and fungivorous nematodes (Fig. 2(b)±(c)).
Bacterivores dominated nematode communities in
both mulch and no mulch treatments and their contribution to the total nematode community ranged
between 48% and 76% (data not shown). Bacterial
feeders showed an immediate but short-lived numerical response to mulch additions (Fig. 2(b)). Bacterial-

feeding taxa signi®cantly contributing to this trend
were Rhabditidae and Cephalobus (Fig. 3(a) and (b)).
Acrobeles, Acrobeloides, Eucephalobus, and Teratocephalus were either always or almost always more
abundant in mulch-free plots (Fig. 3(c)±(f)). Plectus,
however, was always more numerous in mulch-treated
plots (Fig. 3(g)). Wilsonema tended to prefer mulchin¯uenced environments from the midpoint of the
experiment (Fig. 3(h)). Other bacterivores (Alaimus,
Chronogaster, Heterocephalobus, Monhystera, Prismatolaimus, and Zeldia) were not affected by mulch
treatments.
Fungivorous nematodes were more abundant in
mulch-treated plots but only after the second compost
addition (May 1997) (Fig. 2(c)). This effect was
detectable for at least seven months until December
1997. A similar relationship was observed when fungivores were expressed as a proportion of the entire
nematode community (Fig. 2(e)). Aphelenchus was
the dominant fungivorous genus and thus responsible
for the shape of the trend at the trophic group level

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

75

Fig. 2. Abundance of total nematodes (a), bacterivorous nematodes (b), fungivorous nematodes (c); and omnivorous nematodes per 100 cm3
soil (d). Fungivorous (e) and omnivorous (f) nematodes as a percentage of the total nematode community. Abundance of nematodes associated
with decomposition (g) per 100 cm3 soil in mulch- and non-mulch-treated plots. Arrows indicate times when mulch was applied. Asterisks (*)
indicate significant difference at p  0.05.

(Fig. 4(a)). Aphelenchoides was much less abundant,
however, it responded to both mulch additions,
increasing in numbers immediately after placement
of mulch under the trees in May 1995 and June 1997
(Fig. 4(b)). These population peaks were short-lived
because within the next three months the population
numbers were comparable to those found in mulchfree soils. Other fungal feeders such as Diphthero-

phora and Tylencholaimellus were rather sporadic and
thus no relationship could be detected.
Bacterivores and fungivores taken together as the
nematodes associated with decomposition, showed a
quick increase in abundance upon mulch additions,
however, with time their number decreased, even
below the levels found in treatments without mulch
in May 1996. The second mulch application resulted

76

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

Fig. 3. Abundance of bacterivorous families or genera: Rhabditidae (a), Cephalobus (b), Acrobeles (c), Acrobeloides (d), Eucephalobus (e),
Teratocephalus (f), Plectus (g), and Wilsonema (h) per 100 cm3 soil in mulch- and non-mulch-treated plots. Arrows indicate times when mulch
was applied. Asterisks (*) indicate significant difference at p  0.05.

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

77

Fig. 4. Abundance of fungivorous genera: Aphelenchus (a) and
Aphelenchoides (b) per 100 cm3 soil in mulch- and non-mulchtreated plots. Arrows indicate times when mulch was applied.
Asterisks (*) indicate significant difference at p  0.05.

Fig. 5. Abundance of omnivorous genera: Eudorylaimus (a) and
Aporcelaimellus (b) per 100 cm3 soil in mulch- and non-mulchtreated plots. Arrows indicate times when mulch was applied.
Asterisks (*) indicate significant difference at p  0.05.

in a signi®cant (p  0.05) and more prolonged
response of decomposers (Fig. 2(g)).
Omnivorous nematodes, whether expressed as numbers or percentage of the total nematodes, were nearly
always more common in treatments not exposed to
mulch (Fig. 2(d) and (f)). Omnivores were represented
by Aporcelaimus, Aporcelaimellus, Ecumenicus,
Eudorylaimus, Mesodorylaimus, and Pungentus.
Although not always statistically signi®cant
(p  0.05), Eudorylaimus (Fig. 5(a)) and Aporcelaimellus (Fig. 5(b)) were almost always more numerous
in plots without mulch.
Plant-parasitic nematodes made up 6±20% of the
nematode community, with numbers ranging from 35
to 256 per 100 cm3 (data not shown). As a trophic
group, plant parasites did not respond to compost
treatment in any predictable manner. However, several
genera showed consistent patterns. While Belonolaimus was usually more numerous in plots with mulch
(Fig. 6(a)), Criconemoides was usually less numerous
(Fig. 6(b)). Other plant parasites (Hoplolaimus, Meloidogyne, Pratylenchus, Tylenchulus, Trichodorus, and
Xiphinema) did not reveal signi®cant patterns.
Tylenchidae (predominantly Tylenchus spp.) were
considered as root associates (Yeates et al., 1993a).

Within the ®rst half of the experiment these nematodes
were more numerous in soils without mulch, but after
the second mulch application the pattern reversed
(Fig. 6(c)).
Predators and algivores were uncommon in our
soils and on many occasions were completely absent.
On average, their numbers ranged between 0 and 5 per
100 cm3 soil (data not shown).
3.2. Ecological indices
Diversity indices such as richness (total number of
genera), Shannon±Weaver trophic diversity, Shannon±
Weaver generic diversity, and Simpson's diversity
were usually higher in treatments free of mulch
(Fig. 7(a)±(d)). The index of dominance (at the generic level) showed the nematode communities more
dominated by few abundant genera in mulch treated
soils (Fig. 7(e)). The ratio of bacterivores and fungivores to herbivores (B‡F/PP) was typically higher in
plots treated by compost especially during the second
half of the experiment (Fig. 8(a)). Fungivore to bacterivore ratio (F/B) (Fig. 8(b)) could differentiate
mulch from non-mulch treatments only after the second mulch addition. From June 1997 to December

78

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

Fig. 6. Abundance of herbivores: Belonolaimus (a), Criconemoides
(b) and root associates (Tylenchidae) (c) per 100 cm3 soil in mulchand non-mulch-treated plots. Arrows indicate times when mulch
was applied. Asterisks (*) indicate significant difference at
p  0.05.

1997, F/B was signi®cantly (p  0.05) higher in soils
exposed to municipal waste compost. The maturity
indices were nearly always greater in plots without
mulch (Fig. 9(a)±(c)).
3.3. Other measured variables
Soil moisture was always higher in soils covered
with mulch (Fig. 10(a)). Phytophthora nicotianae was
temporally variable and was not suppressed by compost treatments. On two occasions, the numbers of P.
nicotianae were signi®cantly (p  0.05) higher in
mulched plots (Fig. 10(b)). Although not signi®cantly
different, total fungal populations in soils receiving
mulch were slightly higher than in soils treated
with herbicide (40 and 36  102 CFU/g DW soil,

Fig. 7. Indices of diversity: richness (a), Shannon±Weaver trophic
diversity (b), Shannon±Weaver genus diversity (c), Simpson genus
diversity (d), and Simpson genus dominance (e) in mulch- and nonmulch-treated plots. Arrows indicate times when mulch was
applied. Asterisks (*) indicate significant difference at p  0.05.

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

79

Fig. 8. Bacterivores ‡ fungivores to herbivores ratio (a) and
fungivores to bacterivores ratio (b) in mulch- and non-mulchtreated plots. Arrows indicate times when mulch was applied.
Asterisks (*) indicate significant difference at p  0.05.

respectively) in June 1997 (a week after mulch application). Three months later, however, the scenario was
reversed (25 and 34  102 CFU/g DW soil). Bacterial
populations were not affected by the mulch treatment.
Mulch had a positive effect on fruit yields. Every
year, signi®cantly (p  0.05) more fruit yield (28±
33%) was harvested from trees treated with mulch
(Fig. 10(c)).
The mulch layer under the tree canopy was not
effective in controlling weeds. Usually, they were so
abundant that the ground surface under the tree was
not visible. The plots treated with herbicide occasionally had some weeds present, however, not nearly as
abundant as the mulched plots. The following weeds
were present: Virginia pepperweed (Lepidium virginicum), spanish needles (Bidens spp.), Florida purslane (Richardia scabra), old®eld toad¯ax (Linaria
caudensis), common chickweed (Stellaria media), and
bristly starbur (Acanthospermum hispidium).

4. Discussion
Of the three types of citrus orchard management
practices investigated in this study (irrigation, fertili-

Fig. 9. Maturity indices: plant-parasitic index (a), maturity index
(b), and total maturity index (c) in mulch- and non-mulch-treated
plots. Arrows (*) indicate times when mulch was applied. Asterisks
indicate significant difference at p  0.05.

zation, and under the tree ground cover), application
of compost material had the most pronounced effects
on soil nematodes and nematode community structure.
Various genera exhibited different preferences for
their microhabitats, suggesting their unique contributions to the soil ecosystem processes. We categorized
the different responses to compost applications as
three types: I, II, and III.
4.1. Type I response
At the generic or family level, the bacterial-feeding
nematodes, Rhabditidae and Cephalobus showed a
typical r-selected behavior, with sudden and temporal
population increase (within 3±4 weeks) upon mulch
additions. This pattern con®rms ®ndings of other

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D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

Fig. 10. Soil moisture (a), Phytophthora density (CFU/10 g soil)
(b), and primary production (fruit yield) (c) in mulch- and nonmulch-treated plots. Arrows indicate times when mulch was
applied. Asterisks (*) indicate significant difference at p  0.05.

studies on the relationships between organic inputs,
micro¯ora, and bacterivorous nematodes. Typically,
organic inputs trigger quick increase of bacterial
populations followed by a quick increase of some
of the bacterivorous nematodes (Ettema and Bongers,
1993; Ferris et al., 1996; Wasilewska and Bienkowski,
1985; Yeates et al., 1997). As soon as easily decomposable substrates diminish, bacterial and then nematode populations decline usually reaching previous or
even lower populations levels. While Rhabditidae
showed a similar pattern in organic farming systems
in California, Cephalobus did not (Ferris et al., 1996).
Rhabditidae as strict colonizers (c±p ˆ 1) (Bongers,
1990) seem to be affected predominantly by sudden
¯ushes of food resources. Other factors that might be
involved in changing the soil microhabitat appear to be
less important. This might be the reason why rhabdi-

tids are so insensitive to environmental stressors such
as pollutants. Cephalobus, on the other hand, characterized by Bongers (1990) as not as strong a colonizer (c±p ˆ 2) might respond more to a combination
of factors (abundance and type of food, effects of
organic material on soil temperature and moisture,
natural soil characteristics, etc.). Otherwise, Cephalobus, and probably other nematodes, would require
some revisions regarding their c±p classi®cation. Differences in species of Cephalobus and environmental
conditions of Florida and California may account for
these behavioral differences as well.
Aphelenchus and Aphelenchoides (fungal-feeding
nematodes) also showed a type I response. Interestingly, both genera are not considered strict colonizers
(c±p ˆ 2), yet in our experiment they behaved like
typical r-strategists. Results obtained by Ferris et al.
(1997) and Yeates et al. (1993b) did not indicate any
time±organic input relationship. Wasilewska and
Bienkowski (1985), however, observed a delayed
numerical response of fungal feeding nematodes to
organic matter applications. They suggested that the
time-gap between density peaks of bacterial and fungal-feeding nematodes re¯ected slower fungal than
bacterial population build-up. Lack of the delay
response in our study could result from the type
and decomposition state of organic matter. Our
well-decomposed mulch probably contained much
higher initial bacterial and fungal populations than
the dry hay (residues of summer barley) used by
Wasilewska and Bienkowski (1985). Since no waiting
period for micro¯ora (fungi in particular) build-up was
necessary, an immediate response of fungivorous
nematodes was observed. Also, the much lower
C : N ratio of the municipal waste compost (compared
to barley straw) probably facilitated fungal colonization and proliferation.
Aphelenchus, unlike Aphelenchoides, was not
affected by the ®rst mulch application. It is possible
that Aphelenchoides, typically a more common fungivore, may have less specialized feeding habits than
Aphelenchus. If this were the case, the increase of
fungus of any type might immediately be re¯ected in
increased nematode density. Unfortunately, the fungal
composition of the compost used in these two applications was not determined.
No genera from any other trophic groups could
be characterized by the type I response. Typically,

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

bacterial- and fungal-feeding nematodes are associated with decomposition and nutrient mineralization
processes (Freckman, 1988; Ingham et al., 1985).
Higher densities of type I response nematodes may
indicate increased rates of decomposition, possibly
resulting in improved mineralization of nitrogen and
other nutrients.
4.2. Type II response
The bacterial-feeding genera Acrobeles, Acrobeloides, Eucephalobus, and Teratocephalus were generally suppressed by the presence of compost. Since
no temporary numerical response to mulch additions
was observed, environmental factors rather than food
abundance seem to shape the population dynamics of
these bacterivores. Acrobeles and Acrobeloides were
also more numerous in tomatoes grown in conventional than in organic systems (Ferris et al., 1997). The
suppression by mulch of preferred food types (speci®c
bacteria) is unlikely because a signi®cant time  mulch interaction for Acrobeloides and Eucephalobus was found. Lower nematode abundance in
mulch treated soils could be seen in the context of
biological control agents coming down from the
mulch layer (nematophagous fungi and bacteria). This
scenario, however, seems questionable because no
distinct differences between mulched and nonmulched plots in fungal and bacterial population
densities were found. Moreover, virtually no nematodes colonized by fungus, and very few nematodes
colonized by bacteria (Pasteuria spp. mostly on
Meloidogyne) were observed. Differences between
mulched and non-mulched plots in several attributes
of soil chemistry (concentrations of Ca and Na, pH,
organic matter content, and cation exchange capacity)
related to densities of type II response bacterial feeders (Porazinska et al., in preparation), indicating the
chemical component of the soil ecosystem as an
important factor modeling nematode populations.
Teratocephalus is a unique bacterial feeder. It is
considered a K-strategist (c±p ˆ 3). Presence of compost dropped this nematode to almost undetectable
levels. Its density decline in mulch-free plots in the
second half of the experiment probably illustrated the
unusually dry spring and summer of 1997. McSorley
(1997) observed strong positive correlation between
rainfall and Teratocephalus density in citrus orchards.

81

In addition, mulch used in our experiment was a
municipal solid waste, which contained relatively high
concentration of copper. Several recent microcosm
studies investigated the effects of pollutants on soil
nematodes and concluded that copper concentrations
higher than 100 mg gÿ1 result in the reduction of
nematode abundance (Parmelee et al., 1997; Korthals
et al., 1996). On the other hand, Cu is typically bound
in non-bioavailable form at high pH, high concentrations of Ca, and high organic matter content.
Besides the above-mentioned bacterial feeders, we
found Aporcelaimellus and Eudorylaimus (omnivores)
and Criconemoides (an herbivore) all exhibiting the
type II response. Porazinska et al. (1998a) found
higher densities of the two omnivorous genera in
treatments exposed to higher irrigation intensities.
They suggested that higher levels of irrigation were
stabilizing the highly variable water and temperature
soil environments of sandy soils in Florida. Since the
mulch layer contributed to the maintenance of higher
soil moisture, lower densities of Aporcelaimellus and
Eudorylaimus were somewhat surprising. We suspect
that this response difference was associated with the
location of experimental sites. While the irrigation
study (Porazinska et al., 1998a) was carried out on a
site with a slight slope and soils practically never
water saturated, this experiment was carried out on
lands at a lower elevation, occasionally exceeding
water ®eld capacity. Therefore, soil water content
(here less important) could be overridden by other
environmental factors. Korthals et al. (1996) found
omnivorous and predatory nematodes the most sensitive taxa that are negatively affected by copper, nickel,
and zinc added to the soil at a concentration of
100 mg kgÿ1. Although concentrations of heavy
metals in the mulch were relatively high, their concentrations in the soil solutions were minimal (unpublished data). In addition, the negative effect of heavy
metals on nematodes through biomagni®cation is
unlikely because of high soil pH and Ca concentrations (unpublished data), locking heavy metals in nonbioavailable forms.
Criconemoides was suppressed in mulch in¯uenced
environments despite availability of host plants
(weeds). The suppressive effect of organic materials
on ring nematodes has not been reported often (McSorley and Gallaher, 1995, 1996). Usually, organic
amendments have little effect on ring nematodes.

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D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

In general, nematodes showing type II response
may indicate the overall status or quality of the soil
environment. They probably relate to a combination of
food resources and chemical and physical characteristics of their immediate surrounding rather than food
availability exclusively.
4.3. Type III response
Only three genera were placed in this group: Plectus
and Wilsonema representing bacterivorous nematodes,
and Belonolaimus representing plant-parasitic nematodes. In general, presence of mulch created more
suitable soil microhabitats hence supporting higher
abundances of the type III response nematodes. As in
type II response, immediate food availability from
mulch additions did not seem to be a key factor
affecting population densities. Plectus and Wilsonema
are known as aquatic nematodes favoring wetter habitats. Since soil moisture was higher in mulch treated
plots, it is possible that water content was an important
factor in providing microhabitats favorable for Plectus
and Wilsonema. Belonolaimus also appears to respond
more to soil water status than, for instance, to weed
abundance. Indeed, weed growth was much greater in
compost treatments hence possibly supporting higher
populations of Belonolaimus. However, the last two
sampling dates (September and December 1997)
revealed a profound decline in population density of
this nematode which may resulted from saturated with
water soils. The rainfall for the autumn of 1997 was
unusually high, leaving soil saturated with water for
many days. Water-logged soils after two to three days
may become oxygen de®cient and stimulate sulfatereducing bacteria to produce sulfur compounds toxic
to Belonolaimus (Hollis and Rodriguez-Kabana,
1965).
Again, the type III response nematodes may re¯ect
some aspects (different from those indicated by the
type II response nematodes) of the chemico-physical
characteristics of the soil environment rather than
availability of food resources.
4.4. Trophic groups
The patterns observed at the trophic group level for
bacterivores, fungivores, and omnivores resembled
patterns of nematodes at the generic level. For exam-

ple, the density peaks in May 1995 and June 1997 for
bacterial feeders were driven by the most abundant
rhabditids responding to mulch additions. Higher
nematode densities in non-mulch treated plots
between the above-mentioned peaks manifested the
densities of the type II response nematodes (Acrobeles, Acrobeloides, Eucephalobus, and Teratocephalus). Although the pattern at the trophic level can
identify increased abundance and thus activity of
nematodes, in general it does not provide suf®cient
information about the `players' and possible causes of
the observed trends. Trophic group expresses an average response often neutralizing opposite `roles' of
individual species in the soil ecosystem processes.
The different responses of nematodes such as Rhabditidae and Plectus would not be clear at the trophic
group level of resolution. Ferris et al. (1997) provided
evidence for different contributions of bacterivorous
nematode species to N-mineralization. Different
responses of constituent species in the nematode
community may indicate their unique and thus critical
participation in nutrient and energy ¯ow on a temporary scale. This type of knowledge becomes evident
at a level of resolution greater than trophic group.
The pattern formed by fungivorous nematodes was
shaped by Aphelenchus. Again, higher abundance of
Aphelenchus overshadowed the response trend formed
by Aphelenchoides and other fungal-feeding nematodes. Lack of data on precise feeding preferences of
these nematode species and their contributions to
nutrient cycling limits our understanding of the roles
of these fungivores. Based on ®ndings of Ferris et al.
(1997), however, we speculate that fungivores, like
bacterivores, differ in their ability to mineralize nitrogen, thus information on the individual genera or even
species seems more appropriate.
The resolution of the trophic group for omnivorous
nematodes may seem more appropriate in de®ning soil
ecosystem status. Usually relatively low densities of
omnivorous nematode genera or species, however,
limit observation of clear responses induced by environmental changes at the species or genus level. A
natural tendency is to group them in a functional
assemblage, so that magni®ed abundance is more
likely to reveal a response pattern. As typical Kstrategists, omnivores, unlike bacterivores, display
more or less similar environmental preferences. Here,
although genera such as Ecumenicus or Mesodorylai-

D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

mus did not indicate any effects from mulch, at the
level of a functional group they neither masked nor
diluted patterns revealed by Eudorylaimus and Aporcelaimellus. In addition, lack of temporal effects of
mulch (despite the density increase of micro¯ora and
type I response nematodes) on either genus indicates
that trophic level provides information similar to
genus level. However, because of the limited knowledge on the biology and role of these nematodes in soil
processes, we may learn more by monitoring generic
or species composition.
4.5. Ecological indices
The idea of using ecological indices as indicators of
ecosystem quality (e.g. diversity, stability, and resilience) has received increased attention over the last
decade. Indices may be useful tools because they not
only provide quantitative means to characterize an
ecosystem, but also to compare different ecosystems.
Previous studies that used ecological indices to
express changes in the soil environment induced by
various farming tactics include: Ferris et al., 1996;
Freckman and Ettema, 1993; McSorley and Frederick,
1966; Porazinska et al., 1998a; Yeates and Bird, 1994;
and Yeates et al., 1997.
We assume that condensation of taxonomic characterization of the nematode community into a simple
ecological index value should provide convenient
means for inferences about soil ecosystems (status
and processes). In our study, several ecological indices
illustrated nematode community changes induced by
mulch application. None of the measures, however,
could detect any treatment differences due to irrigation or fertilization level (even though a few differences were noticed at the genus and trophic level).
Species richness can enhance ecological resilience
(Peterson et al., 1998). Functions of lost or extinct
species theoretically can be continued by ecologically
similar species. Generally, lower richness in mulch
treated plots re¯ected probably an absence of mononchid and chromadorid genera. Inability to indicate
temporary effects of mulch through time, however,
makes this index imprecise and insensitive for describing soil nematode community changes.
Lower trophic diversity in mulch treatments
resulted from nematode communities predominated
by bacterial and fungal feeders. This inference, how-

83

ever, would be impossible if information about the
generic and trophic composition was unavailable.
Simpson's and Shannon±Weaver diversity indices
can be used interchangeably despite the scale differences (Porazinska, 1998). Here, both indices had very
similar patterns throughout the entire time of the
experiment. They both ¯uctuated more in mulch
treatments, and both responded to temporary changes
due to mulch additions (decrease of diversities). These
indices seem to be more informative than the other
indices just described, although no qualitative inference could be made. Does a decline of a diversity
index indicate loss of ecosystem stability and quality
only? A ¯uctuating nematode diversity index might
re¯ect the dynamics of the ecosystems processes such
as, for instance, temporary changes of decomposition
and nutrient mineralization rate. Organic matter inputs
typically stimulate an increase of microbial populations, that can be followed by a quick increase of their
grazers (Ferris et al., 1996; Wasilewska and Bienkowski, 1985). As the easily degradable organic compounds are used up, microbial populations decline as
do their grazers. The rate of decomposition is related
to the abundance of micro¯ora and their grazers
(Wardle and Lavelle, 1997). Different genera of bacterial feeding nematodes respond variably to changes
of the microbial biomass. Only a few r-strategy
oriented genera can increase rapidly and temporarily
dominate the entire nematode community, negatively
in¯uencing nematode diversity indices (Ferris et al.,
1996). However, to be precise about the reasons of the
deviations of the diversity index value, a more detailed
knowledge of the parties of the community in question
is required. The same argument applies to Simpson's
dominance. Without prior generic characterization of
nematode communities, it would be impossible to
know that an increase of dominance after mulch
additions was due to higher proportions of rhabditids
and aphelenchids.
The fungivorous-to-bacterivorous nematode ratio
can re¯ect some aspects of the soil environment. It
can describe contributions of the above trophic groups
to decomposition processes. Similar values of this
ratio in mulch and non-mulch treated soils during
the ®rst two years of the experiment suggest that
breakdown of organic matter was proportionately
assisted by similar decomposer assemblages of nematodes. The low values of the ratio during this time

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D.L. Porazinska et al. / Applied Soil Ecology 13 (1999) 69±86

indicates predominant contribution of bacterial feeders to decomposition and relatively quick turnover of
the available organic matter (leaf litter, dropped fruit,
decaying weeds, compost). During the third year of
the experiment, changes of the soil environment following compost addition resulted in proportional
shifts of nematodes associated with decomposition.
An increased ratio indicated a switch to fungal pathway and possibly slower rate of organic matter turnover. Higher proportions of fungal-feeding nematodes
probably re¯ected more favorable soil moisture
microhabitats for fungi. Although the ratio helps to
indicate the parties involved in the process of decomposition, it failed to recognize the intensity of the
process. Since the information about the effects of
mulch on densities of type I nematodes and densities
of both trophic groups are compressed the ratio inadequately illustrated the differences between the treatments.
Maturity indices seem to offer better prospects for
detecting and suf®ciently illustrating changes in the
soil environment (Bongers, 1990; Yeates, 1994).
Unlike diversity measures, maturity indices contain
both quantitative and biological-ecological aspects of
the individual nematode species comprising a community. However, low values of maturity indices may
be associated with either rare K-strategists or predominant r-selected nematodes. In our experiment, both
scenarios could explain the patterns of both maturity
indices: MI (Bongers, 1990) and TMI (Yeates, 1994).
Generally, lower MI and TMI in mulch treatments
resulted from suppression of K-selected omnivores,
indicating overall mulch effect on soil environment
over a longer time scale. Signi®cant short-lived
declines of MI and TMI values after mulch application
illustrated increased abundances and activities of the
type I nematodes. Therefore, MI and TMI may be
indicative of temporary intensi®ed decomposition and
nutrient mineralization processes. Similar results were
recorded by Ferris et al. (1996) for conventional and
organic farming systems in California. Lower maturity
of organic plots after incorporation of organic material
was associated with relatively higher proportions of
opportunistic nematodes responding to bacterial
blooms.
Although a measure of maturity index may be
appealing for monitoring purposes, we suggest they
cannot be taken out of the context of agricultural

management practices. Soils with high maturity
indices could be interpreted as more stabilized and
thus more desirable for agricultural endeavors. In our
previous work (Porazinska et al., 1998b), we found
highest maturity indices in treatments with the most
intensive irrigation schemes. Considering water conservation issues and relatively lower productivity and
pro®tability of those treatments, higher maturity
indices would not be advantageous. The same idea
applies to this experiment. Despite higher density of
the citrus root rot fungus (Phytophthora) and higher
weed abundance, productivity of mulch-treated trees
was always greater, while maturity indices had exactly
the opposite pattern. At the current state of knowledge,
it would be rather risky to blindly infer about the
quality or sustainability of the soil ecosystem from a
particular maturity index value. Low maturity indices
may more re¯ect the intensity of soil processes
(decomposition, mineralization) instead of simply
the level of disturbance or degradation.

5. Conclusions
Nematode community measures were useful in
providing the information about the status and processes of the citrus soil ecosystem. They could re¯ect
ecosystem differences imposed by several farming
management practices. A majority of nematode genera and ecological measures could indicate environments in¯uenced by mulch, but not by water or
fertilization level. To accurately characterize the status
and pr